Forelimb kinematics and motor patterns of the slider turtle (Trachemys scripta) during swimming and walking: shared and novel strategies for meeting locomotor demands of water and land

Abstract

SUMMARYTurtles use their limbs during both aquatic and terrestrial locomotion, but water and land impose dramatically different physical requirements. How must musculoskeletal function be adjusted to produce locomotion through such physically disparate habitats? We addressed this question by quantifying forelimb kinematics and muscle activity during aquatic and terrestrial locomotion in a generalized freshwater turtle, the red-eared slider (Trachemys scripta), using digital high-speed video and electromyography (EMG). Comparisons of our forelimb data to previously collected data from the slider hindlimb allow us to test whether limb muscles with similar functional roles show qualitatively similar modulations of activity across habitats. The different functional demands of water and air lead to a prediction that muscle activity for limb protractors (e.g. latissimus dorsi and deltoid for the forelimb) should be greater during swimming than during walking, and activity in retractors (e.g. coracobrachialis and pectoralis for the forelimb) should be greater during walking than during swimming. Differences between aquatic and terrestrial forelimb movements are reflected in temporal modulation of muscle activity bursts between environments, and in some cases the number of EMG bursts as well. Although patterns of modulation between water and land are similar between the fore-and hindlimb in T. scripta for propulsive phase muscles (retractors), we did not find support for the predicted pattern of intensity modulation, suggesting that the functional demands of the locomotor medium alone do not dictate differences in intensity of muscle activity across habitats. Supplementary material available online at

Forelimb muscle function in pig-nosed turtles,Carettochelys insculpta: testing neuromotor conservation between rowing and flapping in swimming turtles

“…Bipolar stainless steel fine-wire electrodes (0.05 mm diameter, California Fine Wire Co., USA) were implanted percutaneously into target muscles of the left forelimb of Carettochelys (see [6] for details) and Apalone (see [5] for details) to generate data for comparison to other species. Protocols differed only slightly for the species; in particular, Carettochelys received local anaesthetic (lidocaine) at implant sites and were tested the same day, whereas Apalone was anaesthetized with ketamine prior to implants and tested the following day.…”

“…Although more accurately viewed as points along a continuum, rowing is characterized by anteroposterior oscillatory motions of paddle-shaped appendages, whereas flapping is characterized by dorsoventral oscillatory motions of wing-shaped appendages [1]. Rowing and flapping have been documented among diverse taxa, including fishes [1][2][3], turtles [4][5][6], birds [7] and mammals [8,9]. Understanding how new locomotor modes arise, whether through changes in morphology, muscle activity or a combination of both, is a major focus of evolutionary studies of musculoskeletal function.…”

“On the Fence” versus “All in”: Insights from Turtles for the Evolution of Aquatic Locomotor Specializations and Habitat Transitions in Tetrapod Vertebrates

“…The rowing strokes of species living ''on the fence'' between aquatic and terrestrial habitats are broadly similar in kinematics to the steps they take on land, in that both involve predominantly anteroposterior movements of the limbs (Davenport et al 1984;Fish 1996;Gillis and Blob 2001;Pace et al 2001;Blob et al 2008;Rivera and Blob 2010). However, flapping strokes of hyperspecialized taxa that have moved ''all in'' to aquatic habitats are reoriented from this plesiomorphic pattern, such that motion is predominantly dorsoventral (Davenport et al 1984;Renous and Bels 1993;Wyneken 1997;Walker and Westneat 2000;Rivera et al 2011a).…”

“…Following published protocols (Loeb and Gans 1986;Blob et al 2008;Rivera and Blob 2010;Schoenfuss et al 2010), we inserted bipolar, fine-wire electrodes to test the actions of five target muscles that, based on their anatomical positions (Walker 1973), were predicted to control all major planes of forelimb motion during swimming. These muscles included coracobrachialis (predicted humeral retractor), pectoralis (predicted humeral retractor and depressor), latissimus dorsi and deltoideus (predicted humeral protractors and elevators) Fig.…”

“…Taxa that have recently invaded aquatic habitats, or that still make frequent use of terrestrial habitats, typically move their limbs with predominantly anteroposterior (i.e., fore-aft) oscillations that include distinct recovery and power strokes, producing a rowing motion that broadly resembles patterns retained from terrestrial kinematics (Davenport et al 1984;Fish 1996;Walker and Westneat 2000;Rivera and Blob 2010). However, taxa that have become highly specialized for life in water often show predominantly dorsoventral (i.e., up-down) oscillations of the limbs, producing flapping motions through which propulsive forces may be generated during both the up-and downstrokes (Vogel 1994;Walker and Westneat 2000;.…”